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Almost there: transmission routes of bacterial symbionts between trophic levels.

Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, Kelly SE, Asplen MK, Hunter MS - PLoS ONE (2009)

Bottom Line: Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries.However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only.In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel. chiel@email.arizona.edu

ABSTRACT
Many intracellular microbial symbionts of arthropods are strictly vertically transmitted and manipulate their host's reproduction in ways that enhance their own transmission. Rare horizontal transmission events are nonetheless necessary for symbiont spread to novel host lineages. Horizontal transmission has been mostly inferred from phylogenetic studies but the mechanisms of spread are still largely a mystery. Here, we investigated transmission of two distantly related bacterial symbionts--Rickettsia and Hamiltonella--from their host, the sweet potato whitefly, Bemisia tabaci, to three species of whitefly parasitoids: Eretmocerus emiratus, Eretmocerus eremicus and Encarsia pergandiella. We also examined the potential for vertical transmission of these whitefly symbionts between parasitoid generations. Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries. However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only. Consequently, Rickettsia is not vertically transmitted in Eretmocerus wasps, a result supported by diagnostic polymerase chain reaction (PCR). In contrast, Rickettsia proved to be merely transient in the digestive tract of Encarsia and was excreted with the meconia before wasp pupation. Adults of all three parasitoid species frequently acquired Rickettsia via contact with infected whiteflies, most likely by feeding on the host hemolymph (host feeding), but the rate of infection declined sharply within a few days of wasps being removed from infected whiteflies. In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding. This study demonstrates potential routes and barriers to horizontal transmission of symbionts across trophic levels. The possible mechanisms that lead to the differences in transmission of species of symbionts among species of hosts are discussed.

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Rickettsia (white arrows) in Er. eremicus follicular epithelial cell (FC).The gap between the follicular epithelial cell and the oocyte (the transition zone - TZ) is due to oocyte resorption. N-nucleus; EnC- endochorion; ExC- Exochorion; VE- Vitellin envelope.
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pone-0004767-g004: Rickettsia (white arrows) in Er. eremicus follicular epithelial cell (FC).The gap between the follicular epithelial cell and the oocyte (the transition zone - TZ) is due to oocyte resorption. N-nucleus; EnC- endochorion; ExC- Exochorion; VE- Vitellin envelope.

Mentions: Electron micrographs of Er. eremicus reveal the presence of bacteria inside the ovaries, within follicular epithelial cells, but not within the oocytes (Fig. 4). Bacteria were also seen right outside the ovary, adjacent to the tunica propria, the ovarian envelope (Fig. 5). The germarium also shows bacteria among stem-, pre-follicle-, and nurse cell nuclei (Fig. 6). The determination that these bacteria are Rickettsia is supported by: 1) Denaturating gradient gel electrophoresis (DGGE) analysis of the bacteria present in Er. eremicus using general 16S rRNA primers that target most known bacteria. A single band, corresponding to Rickettsia was found in this analysis (data not shown). 2) Diagnostic PCR using specific primers designed for B. tabaci symbionts (Hamiltonella, Wolbachia, Cardinium, Arsenophonus and Rickettsia) showed bands only for Rickettsia in the Er. eremicus, as well as for the positive controls in all other cases (data not shown).


Almost there: transmission routes of bacterial symbionts between trophic levels.

Chiel E, Zchori-Fein E, Inbar M, Gottlieb Y, Adachi-Hagimori T, Kelly SE, Asplen MK, Hunter MS - PLoS ONE (2009)

Rickettsia (white arrows) in Er. eremicus follicular epithelial cell (FC).The gap between the follicular epithelial cell and the oocyte (the transition zone - TZ) is due to oocyte resorption. N-nucleus; EnC- endochorion; ExC- Exochorion; VE- Vitellin envelope.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC2651630&req=5

pone-0004767-g004: Rickettsia (white arrows) in Er. eremicus follicular epithelial cell (FC).The gap between the follicular epithelial cell and the oocyte (the transition zone - TZ) is due to oocyte resorption. N-nucleus; EnC- endochorion; ExC- Exochorion; VE- Vitellin envelope.
Mentions: Electron micrographs of Er. eremicus reveal the presence of bacteria inside the ovaries, within follicular epithelial cells, but not within the oocytes (Fig. 4). Bacteria were also seen right outside the ovary, adjacent to the tunica propria, the ovarian envelope (Fig. 5). The germarium also shows bacteria among stem-, pre-follicle-, and nurse cell nuclei (Fig. 6). The determination that these bacteria are Rickettsia is supported by: 1) Denaturating gradient gel electrophoresis (DGGE) analysis of the bacteria present in Er. eremicus using general 16S rRNA primers that target most known bacteria. A single band, corresponding to Rickettsia was found in this analysis (data not shown). 2) Diagnostic PCR using specific primers designed for B. tabaci symbionts (Hamiltonella, Wolbachia, Cardinium, Arsenophonus and Rickettsia) showed bands only for Rickettsia in the Er. eremicus, as well as for the positive controls in all other cases (data not shown).

Bottom Line: Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries.However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only.In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding.

View Article: PubMed Central - PubMed

Affiliation: Department of Evolutionary and Environmental Biology, University of Haifa, Haifa, Israel. chiel@email.arizona.edu

ABSTRACT
Many intracellular microbial symbionts of arthropods are strictly vertically transmitted and manipulate their host's reproduction in ways that enhance their own transmission. Rare horizontal transmission events are nonetheless necessary for symbiont spread to novel host lineages. Horizontal transmission has been mostly inferred from phylogenetic studies but the mechanisms of spread are still largely a mystery. Here, we investigated transmission of two distantly related bacterial symbionts--Rickettsia and Hamiltonella--from their host, the sweet potato whitefly, Bemisia tabaci, to three species of whitefly parasitoids: Eretmocerus emiratus, Eretmocerus eremicus and Encarsia pergandiella. We also examined the potential for vertical transmission of these whitefly symbionts between parasitoid generations. Using florescence in situ hybridization (FISH) and transmission electron microscopy we found that Rickettsia invades Eretmocerus larvae during development in a Rickettsia-infected host, persists in adults and in females, reaches the ovaries. However, Rickettsia does not appear to penetrate the oocytes, but instead is localized in the follicular epithelial cells only. Consequently, Rickettsia is not vertically transmitted in Eretmocerus wasps, a result supported by diagnostic polymerase chain reaction (PCR). In contrast, Rickettsia proved to be merely transient in the digestive tract of Encarsia and was excreted with the meconia before wasp pupation. Adults of all three parasitoid species frequently acquired Rickettsia via contact with infected whiteflies, most likely by feeding on the host hemolymph (host feeding), but the rate of infection declined sharply within a few days of wasps being removed from infected whiteflies. In contrast with Rickettsia, Hamiltonella did not establish in any of the parasitoids tested, and none of the parasitoids acquired Hamiltonella by host feeding. This study demonstrates potential routes and barriers to horizontal transmission of symbionts across trophic levels. The possible mechanisms that lead to the differences in transmission of species of symbionts among species of hosts are discussed.

Show MeSH
Related in: MedlinePlus